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From microbes to mammals: Pond biodiversity homogenization across different land-use types in an agricultural landscape

  • Local biodiversity patterns are expected to strongly reflect variation in topography, land use, dispersal boundaries, nutrient supplies, contaminant spread, management practices, and other anthropogenic influences. Contrary to this expectation, studies focusing on specific taxa revealed a biodiversity homogenization effect in areas subjected to long-term intensive industrial agriculture. We investigated whether land use affects biodiversity levels and community composition (alpha- and beta-diversity) in 67 kettle holes (KH) representing small aquatic islands embedded in the patchwork matrix of a largely agricultural landscape comprising grassland, forest, and arable fields. These KH, similar to millions of standing water bodies of glacial origin, spread across northern Europe, Asia, and North America, are physico-chemically diverse and differ in the degree of coupling with their surroundings. We assessed aquatic and sediment biodiversity patterns of eukaryotes, Bacteria, and Archaea in relation to environmental features of the KH,Local biodiversity patterns are expected to strongly reflect variation in topography, land use, dispersal boundaries, nutrient supplies, contaminant spread, management practices, and other anthropogenic influences. Contrary to this expectation, studies focusing on specific taxa revealed a biodiversity homogenization effect in areas subjected to long-term intensive industrial agriculture. We investigated whether land use affects biodiversity levels and community composition (alpha- and beta-diversity) in 67 kettle holes (KH) representing small aquatic islands embedded in the patchwork matrix of a largely agricultural landscape comprising grassland, forest, and arable fields. These KH, similar to millions of standing water bodies of glacial origin, spread across northern Europe, Asia, and North America, are physico-chemically diverse and differ in the degree of coupling with their surroundings. We assessed aquatic and sediment biodiversity patterns of eukaryotes, Bacteria, and Archaea in relation to environmental features of the KH, using deep-amplicon-sequencing of environmental DNA (eDNA). First, we asked whether deep sequencing of eDNA provides a representative picture of KH aquatic biodiversity across the Bacteria, Archaea, and eukaryotes. Second, we investigated if and to what extent KH biodiversity is influenced by the surrounding land use. We hypothesized that richness and community composition will greatly differ in KH from agricultural land use compared with KH in grasslands and forests. Our data show that deep eDNA amplicon sequencing is useful for in-depth assessments of cross-domain biodiversity comprising both micro- and macro-organisms, but has limitations with respect to single-taxa conservation studies. Using this broad method, we show that sediment eDNA, integrating several years to decades, depicts the history of agricultural land-use intensification. Aquatic biodiversity was best explained by seasonality, whereas land-use type explained little of the variation. We concluded that, counter to our hypothesis, land use intensification coupled with landscape wide nutrient enrichment (including atmospheric deposition), groundwater connectivity between KH and organismal (active and passive) dispersal in the tight network of ponds, resulted in a biodiversity homogenization in the KH water, leveling off today's detectable differences in KH biodiversity between land-use types. These findings have profound implications for measures and management strategies to combat current biodiversity loss in agricultural landscapes worldwide.show moreshow less

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Author details:Danny IonescuORCiD, Mina BizicORCiD, Rajat KarnatakORCiD, Camille L. MusseauORCiD, Gabriela OnandiaORCiD, Minoru KasadaORCiD, Stella A. BergerORCiD, Jens Christian NejstgaardORCiD, Masahiro RyoORCiD, Gunnar LischeidORCiD, Mark O. GessnerORCiD, Sabine WollrabORCiD, Hans-Peter GrossartORCiDGND
DOI:https://doi.org/10.1002/ecm.1523
ISSN:0012-9615
ISSN:1557-7015
Title of parent work (English):Ecological monographs
Publisher:Wiley
Place of publishing:Hoboken
Publication type:Article
Language:English
Date of first publication:2022/04/01
Publication year:2022
Release date:2024/06/12
Tag:biodiversity homogenization; eDNA; intensive agriculture; kettle hole;; land use
Volume:92
Issue:3
Article number:e1523
Number of pages:28
Funding institution:German Federal Ministry of Education and Research (BMBF) within the; Collaborative Project "Bridging in Biodiversity Science -BIBS"; [01LC1501]; DFG Eigene Stelle project [BI 1987/2-1, DI 98/3-1]
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
DDC classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Peer review:Referiert
Publishing method:Open Access / Hybrid Open-Access
License (German):License LogoCC-BY-NC - Namensnennung, nicht kommerziell 4.0 International
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